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African Journal of AIDS Research

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Factors associated with HIV infection among sexually experienced adolescents in Africa: a pooled data analysis
Stella Babalola
a a

Johns Hopkins Bloomberg School of Public Health , Center for Communication Programs , 111 Market Place, Suite 310, Baltimore , Maryland , 21202 , United States Published online: 31 Jan 2012.

To cite this article: Stella Babalola (2011) Factors associated with HIV infection among sexually experienced adolescents in Africa: a pooled data analysis, African Journal of AIDS Research, 10:4, 403-414, DOI: 10.2989/16085906.2011.646655 To link to this article: http://dx.doi.org/10.2989/16085906.2011.646655

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African Journal of AIDS Research 2011, 10(4): 403414 Printed in South Africa All rights reserved

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ISSN 16085906 EISSN 17279445 doi: 10.2989/16085906.2011.646655

AJAR

Factors associated with HIV infection among sexually experienced adolescents in Africa: a pooled data analysis
Stella Babalola Johns Hopkins Bloomberg School of Public Health, Center for Communication Programs, 111 Market Place, Suite 310, Baltimore, Maryland 21202, United States Authors e-mail: sbabalol@jhsph.edu
The article examines the factors associated with HIV status among adolescents aged 1519 years in 13 African countries: Cte dIvoire, Democratic Republic of Congo, Guinea, Kenya, Liberia, Mali, Malawi, Rwanda, Sierra Leone, Swaziland, Tanzania, Zambia and Zimbabwe. The data were derived from demographic and health surveys or AIDS indicator surveys conducted between 2004 and 2009. The levels of HIV prevalence among adolescents varied considerably across the countries. There was significantly higher HIV prevalence among female adolescents as compared with their male counterparts. For male adolescents, circumcision was the only variable significantly associated with HIV status. Nonetheless, the data suggest that the association between male circumcision and HIV status may be exaggerated. Indeed, regional-level random effects became insignificant once male circumcision was introduced into the estimated models, indicating a strong correlation between unmeasured regional-level factors and male circumcision. For female adolescents, multiple sexual partnerships, time elapsed since sexual debut, marital status, household wealth, and the regional prevalence of male circumcision were strongly and positively associated with HIV status. Moreover, for female adolescents there appear to be significant unmeasured variables operating at the regional level which influence the levels of HIV infection. The implications of the findings for HIV-prevention programming, policy and research are discussed. Keywords: circumcision, early sexual debut, HIV/AIDS, models, multiple partnerships, prevalence, proximate determinants framework, random effects, surveillance

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Background Despite recent declines in new HIV infections in most countries, HIV and AIDS remains a global health priority. Worldwide, an estimated 33.3 million people were living with HIV at the end of 2009, with about 2.6 million new infections occurring that year (UNAIDS, 2010). Sub-Saharan Africa with its generalised HIV epidemics contributes more than 66% of the global HIV-disease burden although the sub-region is home to less than 12% of the worlds population. Young people aged 1524 years are among the most at risk for HIV (UNAIDS, 2010; Wilson, Wright, Safrit & Rudy, 2010). Young women in sub-Saharan Africa are particularly at risk, contributing disproportionately to the number of people living with HIV (Gouws, Staneckib, Lyerlaa & Ghys, 2008; Gay, Hardee, Croce-Galis, Kowalski et al., 2010; UNAIDS, 2010). The HIV epidemic in sub-Saharan Africa is generalised, with sexual intercourse at the core of the transmission. One implication of the generalised epidemic in Africa is that most young people experience sexual debut in a context of high vulnerability to HIV. Given the median age at sexual debut in most African countries (between 16 and 18 years), it is reasonable to assume that most HIV-positive adolescents have only recently become infected. Given the difficulty of measuring HIV incidence, HIV prevalence among young

people (for example, adolescents aged 1519 years) has often been suggested for use as a proxy for HIV incidence (Zaba, Boerma & White, 2000; Kayirangwa, Hanson, Munyakazi & Kabeja, 2006; Van Griensven, Varangrat, Wimonsate, Tanpradech, Kladsawad, Chemnasiri et al., 2010). Examining the factors associated with HIV prevalence among adolescents can help to strengthen our understanding of the dynamics of HIV incidence. Focusing on HIV infections among adolescents is important for other reasons. The countries of sub-Saharan Africa generally have a young, dynamic age structure, with more than 40% of the population aged less than 15 years. Young people in the age range 1519 years constitute a large proportion of the individuals at risk for HIV infection through sexual transmission. As such, the dynamics of HIV infection among young people have implications for the overall course of the epidemic (Zaba et al., 2000). Moreover, understanding the risk factors for HIV infection among young people will help to ensure that prevention interventions targeting this age group are effective. Effective interventions for young people, who are transitioning from childhood to adulthood, can help to ensure that they are equipped with health-protective attitudes, behaviours and attributes as they grow older and their risk for HIV increases. This article looks at the factors associated with levels of HIV infection among adolescents aged 1519 years in

African Journal of AIDS Research is co-published by NISC (Pty) Ltd and Routledge, Taylor & Francis Group

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13 sub-Saharan African countries. The data were derived from demographic and health surveys or AIDS indicator surveys conducted between 2004 and 2009. The study countries and years of the survey data are: Cte dIvoire (2005), Democratic Republic of Congo (DRC) (2007), Guinea (2005), Kenya (2008/09), Liberia (2006/07), Malawi (2004), Mali (2006), Rwanda (2005), Sierra Leone (2008), Swaziland (2006/07), Tanzania (2007/08), Zambia (2007) and Zimbabwe (2005/06). The difference between this article and the reports of previous research (e.g. Fortson, 2008; De Walque, 2009; Mishra, Medley, Hong, Gu & Robey, 2009) is its unique focus on adolescents and the methodological approach it adopts. Here, a proximate determinants framework and a multilevel approach were methodologically used to control for measured variables at the individual, household and community levels, as well as for unmeasured heterogeneity at the regional level. Conceptual framework Effective HIV-risk-reduction programming requires looking beyond individual-level factors. In addition to sociodemographic and ideational factors, it is important to consider contextual factors, including the social milieu and socioeconomic and structural characteristics that fuel an HIV epidemic. Ideally, interventions should be designed to reflect these considerations. In sub-Saharan Africa, HIV is primarily transmitted through sexual intercourse and the factors that directly influence transmission include multiple sexual partnerships, absence of male circumcision and lack of condom use (Weller & Davis-Beaty, 2002; Ahuja, Werker & Wendell, 2006; Halperin & Epstein, 2007). These direct determinants depend on factors operating at several levels. At the intrapersonal level, education and marital status are among the sociodemographic variables most often examined in the literature in connection with HIV. Evidence of the relationship between level of education and HIV infection is not consistent. Most studies that have examined the link between HIV and education level have found a positive relationship (e.g. Abebe, Schaap, Mamo, Negussie, Darimo, Wolday & Sanders, 2003; Fortson, 2008). A few studies have found a negative relationship (e.g. Glynn, Caral, Buv, Anagonou, Zekeng, Kahindo & Musonda, 2004; Brnighausen, Hosegood, Timaeus & Newell, 2007; Corno & De Walque, 2007). Others still have found no significant relationship (e.g. Glynn et al., 2004; De Walque, 2009). Not only does the type of observed relationship between education level and HIV status depend on the type of analysis performed, it has also been suggested that the relationship may depend on the stage of the HIV epidemic (Gillespie, Kadiyala & Greener, 2007; Jukes, Simons & Bundy, 2008). There is a large body of literature indicating that HIV status is a function of marital status, although the findings have been inconsistent. Most studies have found that marriage constitutes a significant HIV-risk factor, especially for women, probably due to mens extramarital and concurrent sexual relationships (Clark, 2004; Dunkle, Stephenson, Karita, Chomba, Kayitenkore & Vwalika, 2008). Early marriage has been cited as a particular risk factor for women (e.g. Clark, Bruce & Dude, 2006), although some

studies (including at least one cohort study) have suggested that HIV risk is higher in non-marital relationships (Shisana, Zungu-Dirwayi, Toefy, Simbayi, Malik & Zuma, 2004; Brnighausen et al., 2007). Pertaining to the household level, many studies have examined the relationship between socioeconomic status (SES) and HIV using a variety of measures and methodologies. As with education, and for similar reasons, the evidence linking HIV status to SES has not been consistent. Whereas a number of studies have documented a negative link between wealth and HIV status, evidence from recent studies is increasingly drawing attention to a positive wealth gradient in relation to HIV, with richer people being disproportionately affected by infection (Wojcicki, 2005; Lachaud, 2007; Brnighausen et al., 2007; Fox, 2010). Moreover, some studies have demonstrated that wealth is positively associated with certain HIV-risk factors, including multiple sexual partnerships, extramarital sexual relations and premarital sex (Fortson, 2008; Fox, 2010). Some studies focusing on community-level determinants have examined the relationship between place of residence and HIV status and found that urban residence is associated with increased prevalence (Kirunga & Ntozi, 1997; Beegle & De Walque, 2009). A positive relationship between urbanisation and HIV is understandable considering that higher-risk sexual behaviours are likely to be more common in urban areas than in rural areas. The prevalence of male circumcision in the place of residence has also been found to be associated with HIV prevalence; in general, HIV prevalence is lower in regions with a higher level of male circumcision (Moses, Bradley, Nagelkerke, Ronald, Ndinya-Achola & Plummer, 1990; Ahuja et al., 2006). There is increasing recognition of the important role of social and structural factors, including norms, values, relationship networks and social structures. Social and structural factors do not directly influence HIV infection. Nonetheless, they collectively regulate the context in which the practices and sexual behaviours that directly influence HIV infection occur (Auerbach, Parkhurst, Cceres & Keller, 2009). Whereas there has been no consensus on the definition and operationalisation of the social and structural drivers of HIV, the variables in this category which are most often associated with HIV prevalence include stigma and discrimination, economic inequalities, gender inequalities, mobility, and human-rights violations (Krishnan, Dunbar, Minnis, Medlin, Gerdts & Padian, 2008; Adimora & Auerbach, 2010). Many of these factors are difficult to measure and are rarely directly included in models estimating the determinants of HIV prevalence. However, one would expect them to show up as random effects at the appropriate levels. One framework that allows us to organise these multiple influencing factors in a meaningful way is the proximate determinants framework. This framework has its foundation in demography and has been applied in one form or another to the study of demographic processes for decades. Davis & Blake (1956) introduced an analytic framework that recognised 11 biological and behavioural variables through which social and cultural factors can influence fertility. The authors called these variables intermediate determinants and grouped them into three categories: 1) those affecting

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exposure to intercourse, 2) those influencing exposure to conception, and 3) those affecting gestation and successful parturition (Davis & Blake, 1956, p. 212). Building on that seminal work, Bongaarts (1978) was the first to attempt to quantify the link between fertility and the intermediate or proximate determinants. Since then, several authors have adapted the proximate determinants framework to specific health issues, including child survival (Mosley & Chen, 1984) and HIV incidence (Boerma & Weir, 2005). The proximate determinants framework developed by Boerma & Weir (2005) describes three levels of factors influencing the risk of HIV transmission: underlying determinants, proximate determinants, and biological determinants. They defined the underlying determinants as those variables linked with demographic characteristics, the socioeconomic and socio-cultural environment, and programme context. The proximate determinants include individuallevel behavioural factors (e.g. number of partners, coital frequency, sexual mixing, injecting drug use, condom use) and biological factors (e.g. circumcision, viral load, presence of other sexually transmitted infections, etc.). The proximate determinants directly influence the biological determinants of HIV acquisition, including exposure to HIV-infected persons, efficiency of HIV transmission per contact, and the duration of HIV infectivity (Boerma & Weir, 2005). Applying the proximate determinants framework to understand the factors associated with HIV status requires looking at variables at multiple levels, including household, community and societal variables. It also requires being mindful of meaningful causal pathways. Drawing on the proximate determinants framework, this article examines the biological, behavioural and more distal determinants of HIV infection in sub-Saharan Africa. In the estimated models, we controlled not only for the effects of measured variables at various levels but also for random effects at the regional level. Data and methods Data set A pooled analysis of data was performed using the results of demographic and health surveys (with an HIV-testing component) or AIDS indicator surveys variously conducted in 13 countries between 2004 and 2009. The study countries are: Cte dIvoire, Democratic Republic of Congo (DRC), Guinea, Kenya, Liberia, Mali, Malawi, Rwanda, Sierra Leone, Swaziland, Tanzania, Zambia and Zimbabwe. The sampling designs for these surveys were very similar; detailed description of the design for each survey has been provided in the respective reports, which are accessible from the Measure DHS website (<http://www.measuredhs.com/countries>). In general, the surveys were designed to yield data with representativeness at the national or sub-national levels. For some of these surveys (i.e. Cte dIvoire, Liberia, Tanzania, Zambia and Zimbabwe), all the respondents targeted for interview were also eligible for HIV testing. In the other countries, only a subsample (either half or one-third) of the men and women eligible for interview were targeted for HIV testing. In all cases, HIV testing was conducted only after obtaining the respondents informed consent.

The analyses here focus on data for male and female adolescents aged 15 to 19 years. The decision to focus on adolescents is informed by the assumption that they have, for the most part, recently experienced sexual debut and thereby make a considerable contribution to incident HIV infection. Another advantage of focusing on adolescents is that bias due to differential mortality between HIV-infected and uninfected people is not expected to be substantial since the infection is likely to have been recent; the median survival time with HIV has been estimated at 10 to 12 years on average in Africa (Glynn, Sonnenberg, Nelson, Bester, Shearer & Murray, 2007; Todd, Glynn, Marston, Lutalo, Biraro, Mwita et al., 2007). To standardise the effects of sexual experience, we decided to focus on adolescents who reportedly had ever had sex, and as such were exposed to the risk of sexual transmission of HIV. This approach of limiting the analyses to data for people who have experienced sexual debut allows us to focus on sexual transmission of HIV and it has precedence in the literature (e.g. Clark, 2004). The respondents from the 13 study countries included a total of 26 954 male and female adolescents; of these, 11 289 (4 617 males and 6 672 females) were sexually experienced. The numbers of adolescent who reported ever having had sex varied from 411 in Rwanda to 1 416 in Liberia (Table 1). Data analysis The data from the 13 study countries were pooled. Since HIV infection is a relatively rare phenomenon during adolescence, pooling data from several countries provides significant power to analyse the factors associated with an HIV-positive status. Doing analyses for individual countries would have been problematic considering the extremely low level of HIV prevalence in some of the study countries. For example, HIV prevalence among adolescents was estimated at lower than 1% in Guinea, Liberia, Mali, Rwanda and Sierra Leone. Pooling data from several countries might mask significant differences in the factors associated with HIV infection among the countries. However, De Walque (2009) found that although there were some country differences in the factors associated with HIV status in a five-country study, the results were largely consistent across the countries. We first examined variations in the dependent and independent variables across the countries. For these analyses we applied sample weights provided in the datasets. The survey data that we analysed are clustered: individuals are nested within households, households are nested within enumeration areas (EAs), and EAs are nested within regions. An appropriate analytical method should take this nested structure into consideration and allow the partitioning of the residual variance across the various levels of clustering. Using traditional regression methods for nested data would result in underestimating the standard errors of the regression parameters and overestimating the statistical significance of the parameters (Guo & Zhao, 2000). In this article, using multilevel modelling, we examine the fixed effects of variables at the individual, household, community and regional levels; we also examine random effects at the regional level. Drawing

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Table 1: Distribution of the survey respondents aged 1519 years, by country and self-reported sexual-experience status Country Cte dIvoire DRC Guinea Kenya Liberia Mali Malawi Rwanda Sierra Leone Swaziland Tanzania Zambia Zimbabwe All respondents Sexually experienced 1 054 905 772 606 1 416 797 589 411 602 759 1 176 1 197 1 005 11 289 Not sexually experienced 673 858 635 896 807 1 091 420 1 993 473 1 613 2 615 1 180 2 411 15 665 Total 1 727 1 763 1 407 1 502 2 223 1 888 1 009 2 404 1 075 2 372 3 791 2 377 3 416 26 954

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on Boerma & Weir (2005) and following earlier works (e.g. Lewis, Donnelly, Mare, Mupambireyi, Garnett & Gregson, 2007), we estimated three models for each sex: 1) a model assessing associations between HIV status and proximate determinants, 2) a model assessing associations between underlying factors and HIV status, and 3) the full model that includes both proximate determinants and underlying determinants as independent variables. Each of these three models also assessed random effects at the regional level. We estimated the models using the gllamm command in Stata statistical software (see Rabe-Hesketh, Skrondal & Pickles, 2004). To test the hypothesis that the random effects equal zero, we did not use Wald tests since the null value is on the border of the parameter space, given that the value of a variance is never negative. As recommended by Rabe-Hesketh & Skrondal (2008) we used a likelihood ratio test comparing the model to one in which the random effects have been constrained to be equal to zero; we then used half of the traditional p-values to evaluate the significance of the random effects. Variables and measurement Dependent variable The dependent variable in this analysis is HIV serostatus. In all the study countries, HIV testing was anonymous and performed after obtaining informed consent from the respondents. The method for drawing, preserving, and testing the samples was similar in all the study countries. A description of the blood-sample collection, processing and testing protocol is provided in Mishra et al. (2009). It can also be found in the individual country reports, accessible through the Measure DHS website (<http://www. measuredhs.com/countries>). Independent variables We assessed a total of nine independent variables in the various models, which included proximate determinants (i.e. multiple partnerships in the last 12 months, condom use at first sex, male circumcision [for men only], and time elapsed since sexual debut) and underlying determinants (i.e. education, marital status, household SES, place of

residence, and prevalence of male circumcision in region of residence). The independent variables are described below: 1) Circumcision: This variable is included only for the male adolescents. It is derived from a question that asked if the respondent was circumcised. 2) Multiple partnerships in the last 12 months: This variable was derived from the question on the respondents number of sex partners in the last 12 months. We distinguished between sexually experienced individuals who had none or only one sex partner and those who had two or more partners in the last 12 months. 3) Condom use at first sex: We measured this variable as a binary variable contrasting those who reportedly used a condom at the time of first sex with those who did not. 4) Time elapsed since sexual debut: This variable was measured as the difference between current age and age at sexual debut. We distinguished between individuals who had experienced sexual debut less than three years before the survey and their peers who had experienced sexual debut at least three or more years before the survey. 5) Education: We derived this variable from the question on the highest level of education attained. We distinguish between those with a secondary school education or higher and those with a primary school education or less. 6) Marital status: For this variable we used a binary variable that contrasts never-married individuals with ever-married ones. 7) Socioeconomic status (SES): For SES, we used a wealth index based on household assets or living conditions. Specifically, we computed the wealth index as the number of nine possible household assets or attributes: flush toilet, electricity, radio, television, bicycle, refrigerator, motorcycle, car, and a non-earth floor for the dwelling unit. The nine items have an alpha coefficient of 0.74. We derived a categorical variable from this index indicating low, medium or high SES. 8) Place of residence: For the place of residence we used a binary variable that distinguished between urban and rural residents.

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9) Prevalence of male circumcision in the region of residence: We computed this variable as the fraction of male adolescents in a region who are circumcised. The resulting fraction was then divided into tertiles to denote low, medium and high prevalence of male circumcision. In addition to the independent variables described above, the estimated multilevel models also included random effects at the regional level, measuring the influence of unmeasured variables at that level. Results Sexual experience and HIV prevalence Overall, 2.3% of the adolescents in the study countries were HIV-infected. Female adolescents (3.1%) were significantly more likely than their male counterparts (1.3%) to be infected: F = 64.5; p < 0.0001. In each of the study countries, HIV prevalence was higher among female adolescents as compared with male adolescents (data not shown). For female adolescents, sexually experienced individuals were more likely to be HIV-positive than those who were not sexually experienced (4.7% versus 1.7% HIV prevalence). The data reveal no overall difference in HIV prevalence among the male adolescents who were reportedly sexually experienced and their peers who were not (1.4% HIV prevalence for both categories). Actually, in seven countries (Cte dIvoire, Guinea, Mali, Malawi, Swaziland, Tanzania and Zambia) the sexually experienced male adolescents were less likely to be HIV-positive than those who were not sexually experienced. Variations in HIV prevalence and proximate determinants across the countries The prevalence of HIV among the sexually experienced adolescents varied considerably across the 13 study countries (see Table 2). The percentage of adolescents who were HIV-positive ranges from 0.8% in Mali and Sierra Leone to 12% in Swaziland. In general, HIV prevalence was lower in the West African countries than in East Africa or southern Africa. However, there are two noticeable exceptions to this general trend: Rwanda and Tanzania, both countries in East Africa with relatively low HIV prevalence among adolescents, whereas HIV prevalence among adolescents in Cte dIvoire was relatively high for the West African region. As an initial attempt to assess the factors associated with HIV status among adolescents across the countries, we examined differences in selected biomedical and behavioural variables (see Table 2). The variables examined included male circumcision, multiple partnerships in the last 12 months, and condom use at first sex. With regard to condom use at first sex and multiple sexual partnerships, the high-HIV-prevalence countries are not consistently at a disadvantage as compared with the low-HIV-prevalence countries. For example, while Swaziland and Zimbabwe had the highest HIV prevalence among adolescents, they were characterised by relatively low reporting of multiple sexual partnerships. In contrast, some West African countries (e.g. Mali and Liberia, specifically), in spite of their low HIV prevalence among adolescents, were characterised by high

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prevalence of multiple sexual partnerships for both male and female adolescents. In a similar vein, condom use at first sex was less common in the low-HIV-prevalence countries than it was in any of the high-HIV-prevalence countries. Male circumcision was the only variable that seems to have the expected relationship with HIV prevalence at this ecological level: the high-HIV-prevalence countries showed the lowest prevalence of male circumcision. The only exceptions were Rwanda, a country with very low prevalence of male circumcision and very low HIV prevalence, and Cte dIvoire, a country with moderately high HIV prevalence in spite of the near universal practice of male circumcision. With a more critical look at the data in Table 2, it is possible to explain, to some extent, differences in the level of HIV prevalence in the study countries in light of the combination of male circumcision and the two behavioural variables. In essence, it appears that what countries lack in terms one or more protective factors, they compensate for in terms of the others. For example, the potentially negative effect of a low level of male circumcision in Rwanda may be offset by the benefit of a low prevalence of multiple partnerships, resulting in low HIV prevalence. Similarly, in most West African countries, widespread male circumcision probably offsets the potential danger associated with early sexual debut, low condom use at first sex, and high prevalence of multiple sexual partnerships to result in low HIV prevalence. In other words, it appears that, at the aggregate level, a combination of these biomedical and behavioural factors accounts for the levels of HIV prevalence in the study countries. The next section looks at the relative importance of the explanatory variables. Factors associated with HIV status The results of the multilevel logistic regression models that assess the extent to which the variables (enumerated above) were independently associated with HIV status among adolescents are presented in Tables 3 and 4, for males and females, respectively. To assess the pertinence of the decision to use a random-effects model for the data, we first estimated, for each sex, an empty model that has no covariates. For both sexes, the results of the empty model (data not shown) demonstrated that random effects at the regional level were significant for both sexes (males: variance = 0.786, standard error = 0.382, one-sided p < 0.01; females: variance = 1.165, standard error = 0.240, one-sided p < 0.0001), indicating significant heterogeneity in HIV prevalence across the regions. Results for male adolescents It is interesting to note that in contrast to the results of the empty model, as we introduced independent variables in Models 1 to 3, the random effects ceased to be significant suggesting that unmeasured variables at the regional level have no noticeable effects beyond what can be accounted for by the covariates in the model. The lack of significant random effects appears to be due to the presence of individual circumcision status or regional prevalence of male circumcision in the models. Indeed, versions of Models 1, 2 and 3 which excluded the circumcision variables showed significant random effects at the regional level (data not shown).

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Table 2: HIV prevalence and other indicators among sexually experienced adolescents aged 1519 years in selected African countries (CUFS = percentage of the sexually experienced respondents that used a condom at first sex; MC = percentage of the adolescent males that were circumcised; MP12 = percentage of the sexually experienced respondents that had more than one sex partner during the last 12 months) Indicators for male adolescents MP12 CUFS MC 25.6 10.0 96.8 26.3 54.9 95.9 29.3 10.9 98.3 9.9 23.7 73.0 17.0 3.9 97.3 43.5 13.7 99.7 12.6 27.2 22.3 1.2 10.9 13.1 13.2 7.1 92.1 17.8 48.6 3.4 10.5 29.9 65.0 10.5 20.6 12.4 11.9 38.0 11.2 16.8 24.0 59.8 Indicators for female adolescents MP12 CUFS 9.1 4.8 19.7 40.6 9.6 12.2 5.3 28.7 14.0 7.7 20.5 5.3 2.7 21.1 0.01 14.5 8.1 3.1 5.7 52.8 6.5 33.5 5.5 28.6 6.3 23.8 10.0 22.0

Country DRC Cte dIvoire Guinea Kenya Liberia Mali Malawi Rwanda Sierra Leone Swaziland Tanzania Zambia Zimbabwe All countries

HIV prevalence 0.014 0.024 0.010 0.032 0.013 0.008 0.025 0.013 0.008 0.120 0.013 0.058 0.083 0.033

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The results of Model 1 (Table 3) show that male circumcision is the only proximate determinant significantly associated with HIV infection among sexually experienced male adolescents. In this model, male circumcision reduced the odds of HIV infection by a significant 72%. Introducing the underlying determinants in the full model (Model 3) did not change this finding at all. As the results of Model 2 show, with the exception of the regional prevalence of male circumcision, none of the underlying determinants is significantly associated with HIV status. The observed relationship between HIV status and regional prevalence of male circumcision is such that increased prevalence of male circumcision is associated with reduced odds of HIV infection. Results for female adolescents Pertaining to female adolescents, the effects of unmeasured variables at the regional level remain strong even after covariates were introduced into the estimated models. The data clearly show that engaging in multiple sexual partnerships is strongly associated with increased risk of HIV infection. Substantively, having had more than one sexual partner in the last 12 months increased the odds of HIV infection by 79%. Similarly, time elapsed since first sex, a proxy for early sexual debut, is positively associated with the odds of HIV infection. However, the results do not show any significant relationship between HIV status and condom use at sexual debut. As shown in the magnitude and significance of the log-likelihood ratio test comparing Model 2 to the null model, the fixed effects of the underlying determinants included in the model are jointly significant (see Table 4). For female adolescents, being single (never married) significantly decreased the odds of HIV infection whereas education level did not show any significant association. There is a curvilinear relationship with wealth, such that, as compared with low SES, medium socioeconomic level is associated with increased odds of HIV infection whereas high SES is

not. Furthermore, urban versus rural residence is associated with an increased risk of HIV infection. Specifically, female adolescents living in urban areas were 76% more likely to be HIV-infected than were their peers in rural areas. Finally, the data indicate that living in a region where male circumcision is prevalent is protective for female adolescents: the greater the prevalence of male circumcision in the region of residence, the lower the odds of contracting HIV. Inclusion of both the proximate and the underlying determinants in Model 3 did not affect the significance of any of the proximate determinants. Neither did it affect the significant associations between HIV infection and wealth or regional prevalence of male circumcision. However, marital status became less significant and urban residence became more significantly associated with HIV infection. Discussion This article examines the factors associated with HIV prevalence among male and female adolescents aged 1519 years in 13 African countries. Considering the relative rareness of HIV infections among adolescents, pooling data from various countries allows us the power to make inferences concerning the proximate and underlying determinants of HIV infection. Moreover, focusing on late adolescence makes it possible to identify significant correlates of HIV infection among people who are at the earliest stages of sexual exposure to HIV. Indeed, looking at HIV infections among late adolescents has been suggested as an acceptable proxy for understanding HIV incidence. A look at the results concerning the variation in HIV prevalence across the countries and between males and females offers no surprises. Levels of HIV prevalence among adolescents varied considerably across the countries, mimicking cross-country differences in overall HIV prevalence. Female adolescents were more likely to be HIV-infected as compared with their male counterparts. This

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Table 3: Parameter estimates (odds ratio) for the multilevel model for HIV-positive status among male adolescents, adjusting for selected biomedical, sociodemographic, behavioural, household and community variables (RC = absolute risk in the control group) Random effects models Model 2b

Predictor Individual-level sociodemographic, behavioural and biological variables Respondent circumcised: No (RC) Yes Time elapsed since first sex: 2 years or less (RC) 3 years or more Number of sex partners in last 12 months: 0 or 1 (RC) 2 or more Condom use at first sex: Did not use (RC) Used Education: Primary school or less Secondary school or more Marital status: Ever-married (RC) Never married Household-level Indicator Socioeconomic status (SES):1 Low (RC) Medium High Community-level indicator Place of residence: Rural (RC) Urban

Model 1a

Model 3c

1.00 0.28** 1.00 0.95 1.00 0.98 1.00 1.13

1.00 0.26** 1.00 0.97 1.00 0.98 1.00 1.06 1.00 1.23 1.00 1.18

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1.00 1.15 1.00 1.21

1.00 1.57 1.25

1.00 1.57 1.27

1.00 1.45

1.00 1.38

Regional-level indicator Prevalence of male circumcision in region of residence: Low (RC) 1.00 Medium 0.29** High 0.19*** Regional-level random effects2 0.312 (0.283) 0 0.174 (0.304) Log likelihood 278.1 274.7 275.9 Log-likelihood ratio test 16.4*3 23.3*3 20.8*3 Number of level-1 items (individuals) 4 617 Number of level-2 items (region) 120 Notes: a Model with proximate variables only (biological and behavioural). b Model with underlying variables only (sociodemographic, household, community and regional). c Full model with proximate and distal variables. 1 Derived based on nine household assets or attributes: flush toilet, electricity, radio, television, bicycle, refrigerator, motorcycle, car, and non-earth floor for the dwelling. 2 Random effects are expressed as variance; the significance of random effects was evaluated by comparison to a model in which the random effects were constrained to zero using a log-likelihood ratio test; one-half naive p-values used. 3 Compared to the null model. *p < 0.01; **p < 0.001

finding is consistent with what is generally known about HIV infection in sub-Saharan Africa (cf. UNAIDS, 2010). Higher levels of HIV infection among young women as compared with men of the same age group indicate that women are becoming infected at earlier ages than men. This finding also points to age-mixing in sexual relations, with female adolescents often becoming infected by older men. The low

levels of HIV infection among the male adolescents is partly due to later sexual debut and thereby involves a shorter time of exposure to HIV. Our data show that, overall, the median ages at sexual debut were 18.6 years for male adolescents and 17.8 for female adolescents. Indeed, in only five of the 13 study countries (i.e. DRC, Cte dIvoire, Kenya, Zambia and Zimbabwe) was the median age at sexual debut not

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Table 4: Parameter estimates (odds ratio) for the multilevel model for HIV-positive status among female adolescents, adjusting for selected biomedical, sociodemographic, behavioural, household and community variables (RC = absolute risk in the control group) Random effects models Model 2b

Predictor Individual-level sociodemographic, behavioural and biological variables Number of sex partners in last 12 months: 0 or 1 (RC) 2 or more Condom use at first sex: Did not use a condom (RC) Used a condom Time elapsed since first sex: 2 years or less (RC) 3 years or more Education: Primary school or less Secondary school or more Marital status: Ever-married (RC) Never married Household-level indicator Socioeconomic status (SES):1 Low (RC) Medium High Community-level indicator Place of residence: Rural (RC) Urban Regional-level indicators Prevalence of male circumcision in region of residence: Low (RC) Medium High Regional-level random effects:2

Model 1a

Model 3c

1.00 1.79* 1.00 1.05 1.00 1.63**

1.00 1.79* 1.00 1.03 1.00 1.61** 1.00 0.92 1.00 0.67*

1.00 0.89 1.00 0.61**

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1.00 1.52* 1.26

1.00 1.56** 1.27

1.00 1.76**

1.00 1.71**

Log likelihood Log-likelihood ratio test Number of level-1 items (individuals) Number of level-2 items (region) Notes: a Random-effects model with proximate variables only (biological and behavioural). b Random-effects model with distal variables only (sociodemographic, household, community and regional). c Full random-effects model with proximate and distal variables. 1 Derived based on nine household assets or attributes: flush toilet, electricity, radio, television, bicycle, refrigerator, motorcycle, car, and non-earth floor for the dwelling. 2 Random effects are expressed as variance; the significance of random effects was evaluated by comparison to a model in which the random effects were constrained to zero using a log-likelihood ratio test; one-half naive p-values used. 3 Compared to the null model. *p < 0.01; **p < 0.001

1.279** (0.262) 1163.6 24.8**3 6 672 121

1.00 0.29** 0.11** 0.496** (0.169) 1133.6 84.7**3

1.00 0.27** 0.10** 0.489** (0.162) 1122.2 107.63**3

significantly higher for the male adolescents than for the females. Circumcision is the only proximate determinant that was significantly associated with HIV infection in male adolescents. The important protective role of male circumcision has become one of the most widely documented aspects of HIV prevention of this century, although considerable controversy still persists about the justification for, and feasibility of, large-scale circumcision programmes (Muula, 2006; Quinn,

2007; Smith, Taylor, Kilmarx, Sullivan, Warner, Kamb et al., 2010). The absence of regional-level random effects in the proximate-determinants-only model is both surprising and informative. Interestingly, prior to introducing the variable of male circumcision into this model, the random effects were significant. In other words, it appears that rather than being a purely biomedical, individual-level variable, male circumcision has a significant socio-cultural dimension. Indeed, male circumcision is not the result of a random, individual-

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level decision but is a cultural practice. Whereas there is compelling evidence of the benefits of male circumcision from a medical viewpoint, our data suggest that some of the benefits of the practice may be due to other protective sexual practices within the cultural systems where male circumcision is commonly practised. For example, part of the observed association between male circumcision and HIV infection may be due to the effects of religion, religiosity, ethnicity, degree of social conservativeness in the place of residence, social cohesion, traditional practices related to marriage and remarriage, and other factors regulating heterosexual relationships. All of these variables were not measured in the surveys used in the analyses here and were not included in the estimated models. The observed association between male circumcision and HIV infection in this study may therefore be an exaggeration of the true relationship. Further research is required to provide a better understanding of how much of the HIV-protective benefits of circumcision for males is due to its biological properties and how much of it is due to its cultural dimension. For female adolescents, both multiple sexual partnerships and the time elapsed since sexual debut (a reflection of early sexual debut) were negatively associated with HIV infection. These findings were expected and echo what prior studies have found (e.g. Mishra & Bignami-Van Assche, 2009). Many of the underlying determinants are significant for female adolescents. For example, consistent with findings from previous studies, marriage constitutes a significant HIV-risk factor for female adolescents. Early marriage, age-mixing or the tendency for women to marry men who are older and more sexually experienced than themselves, conjugal risk-behaviour asymmetry (e.g. the tendency for married men to engage in extramarital affairs whereas married women do not), a power imbalance within the conjugal family, and other social norms that are unfavourable to women are some of the factors that may explain this finding (cf. Pettifor, Rees, Kleinschmidt, Steffenson, MacPhail, Hlongwa-Madikizela et al., 2005; Wilson et al., 2010). Surprisingly, the findings show that neither multiple sexual partnerships nor time elapsed since sexual debut were significantly associated with prevalence of HIV among the male adolescents. Equally unexpected is that the results offer no evidence that condom use at first sex is significantly associated with HIV infections among either male or female adolescents. Many studies have established a stability effect between condom use at first sex and consistent condom use later on in life (Shafii, Stovel, Davis & Holmes, 2004; Yotebieng, Halperin, Mitchell & Adimora, 2009). Our data reveal a strong correlation between condom use at first sex and condom use at last sex among adolescents who reportedly had been sexually active for more than one year (correlation coefficient = 0.40 for male adolescents and 0.41 female adolescents; p < 0.0001 in both cases). Condoms may offer significant protection against HIV if used consistently (Weller & Davis-Beaty, 2002). However, we found that the adolescents who reportedly used condoms during their first and last sexual encounters were not less likely to be HIV-infected than their peers who either did not use condoms at all or only used a condom for one of the

encounters (data not shown). The finding that condom use was not associated with reduced odds of HIV infection is consistent with the findings of previous studies. For example, Mishra et al. (2009) found a positive link between HIV infection and each of three measures of condom use (ever use, consistent use, and use at last sex) in many of their study countries. The data also reveal a curvilinear relationship between wealth and HIV infection for female adolescents such that high SES does not significantly increase the risk for HIV whereas medium SES does. This result is somewhat different from what other studies in African countries have found (e.g. Mishra et al., 2009). Living in a region with widespread practice of male circumcision appears to be protective for female adolescents although it does not negate the relevance of individual protective behaviours. Taken together, the results suggest the existence of distinct but related HIV epidemics for male and female adolescents. There is an extremely complex epidemic for female adolescents and a less complex one for male adolescents. The factors that place each sex at risk for HIV infection differ; the extent to which contextual and social factors play a role also seem to differ. There is no refuting the fact that a comprehensive approach is required to successfully stem the spread of HIV. Obviously, male circumcision should be part of this comprehensive approach. The study offers compelling evidence that male circumcision offers significant protection for young men and contributes to risk reduction for young women. However, as the findings suggest, male circumcision should be neither the only nor even the most prominent strategy for any country. Promoting male circumcision at the expense of other HIV-prevention strategies would be to neglect the myriad factors that put young women at risk, including the factors that make them engage in multiple sexual partnerships or early sexual debut. Moreover, this study has shown that part of the association between male circumcision and HIV infection may due to unmeasured socio-cultural factors operating at the regional level. Therefore, efforts to promote male circumcision should be mindful of contextual factors, particularly the norms, values, traditional practices and other socio-cultural factors that may compromise the acceptance or limit the effects of male circumcision. Efforts should continue to focus on partner reduction and delay of sexual debut if we are to see significant declines in new HIV infections among women. However, efforts targeting partner reduction and delay of sexual debut should be strategic, based on the best available science on behaviour change and using the most effective communication channels for the intended audience. The significance of random effects at the regional level for female adolescents suggests that efforts to reduce vulnerability to HIV in this group should address the broader social and economic factors that place young women at risk of acquiring HIV. For example, mitigating HIV risk for female adolescents will require addressing gender inequalities that put them at a comparative disadvantage. A human-rights approach is needed to ensure gender equality in access to HIV-prevention information and services and to address the norms and traditional practices that place women at

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risk. Such an approach should also emphasise activities designed to strengthen the capacity of women and female adolescents to negotiate safer sex successfully. Included in such an approach should be activities designed to empower communities to take collective actions to mitigate the HIV risk of its members, especially females. Study limitations This study has some limitations that should be highlighted. Some of these pertain to the measures used to operationalise the independent and outcome variables, while others relate to the nature of the survey data analysed. For example, while HIV status derived from a blood test is an objective measure, a potential source of bias is that not all the respondents who were selected for HIV testing were eventually tested, either because they refused to provide consent or were absent during the survey. If participation in HIV testing once a person had been selected for testing was random, then this issue would be inconsequential. But, in all likelihood, the individuals that accepted to be tested for HIV were different from those who refused the test. We did not examine the sociodemographic or behavioural characteristics of the respondents that were tested as compared to those that were selected for testing but were not tested. However, Mishra, Barrere, Hong & Kahn (2008) evaluated the potential bias due to non-response and the exclusion of non-household population groups in data from 14 African countries. They found that whereas there was evidence that non-tested men and women had significantly higher predicted HIV prevalence than their HIV-tested peers in some countries, the overall effect of non-response on national HIV seroprevalence estimates was negligible. Another limitation of this study is that the behavioural data were based on self-report. Although the implementers of the demographic and health surveys have created guidelines for minimising measurement and other errors, we cannot rule out the possibility of bias due to memory lapse or wilful misreporting. Unfortunately, for most of the variables, it is not possible to assess and correct for the extent of misreporting. Since sexual relations are at the core of the HIV epidemic in Africa, the relationship between sexual experience and HIV serostatus offers an avenue for assessing the quality of the data on sexual experience. All other things being equal, HIV prevalence should be considerably higher among individuals who have had sex as compared with their peers who have not. As discussed earlier, the proportion of adolescents who were reportedly not sexually experienced but who were HIV-positive is not negligible. Moreover, in seven of the 13 study countries, HIV prevalence was higher among male respondents who were reportedly not sexually experienced than among their counterparts who admitted to being sexually experienced. While other sources of HIV infection (e.g. mother-to-child transmission, blood transfusion, contaminated sharp objects) may explain some of the infections among the sexually inexperienced, it is highly unlikely that these sources would account for the observed pattern. This specific finding points to the possibility of the respondents misreporting of sexual activity among the male adolescents. In other words, it is possible that many

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of the male adolescents who reported they had not had sex were actually sexually experienced; the reverse is also possible. We further tested the hypothesis of sexualexperience misreporting by looking at the relationship between male circumcision and HIV status separately for the respondents who were reportedly sexually experienced and those who were reportedly sexually inexperienced. The models controlled for the fixed effects of circumcision, age, urban residence, wealth and education. The models also controlled for random effects at the regional level. All other things being equal, one would expect circumcision to play a considerably greater protective role among sexually experienced men than among those who are not sexually experienced. The results did not confirm this hypothesis. Indeed, circumcision was found to be almost as protective for the sexually inexperienced (odds ratio = 0.304; p < 0.001) as for the sexually inexperienced (odds ratio = 0.256; p < 0.001). It is therefore likely that for the sake of social desirability or other reasons, many of the male adolescents misreported their sexual-experience status. Depending on the direction of this bias, the results presented here may have underestimated or overestimated the observed relationships for male adolescents. For example, it is easy to argue that the underreporting of sexual activity may also extend to the underreporting of the number of sexual partners. In this case, we may be underestimating the relationship between multiple sexual partnerships and HIV status. Other limitations of the study relate to the problems inherent in cross-sectional data: reverse causality and selectivity. For example, HIV status might have a depressing effect on SES such that people with HIV tend to have lower SES due to their inability to be consistently gainfully employed. In addition, higher SES might increase the probability of contracting HIV (incidence) and, at the same time, increase the probability of survival subsequent to infection. Cross-sectional data do not allow us to tease out such complexities. Conclusions Male circumcision was the only variable significantly associated with HIV status among sexually experienced male adolescents. However, the data suggest that the protective benefits of male circumcision may have been exaggerated. Indeed, it is likely that the association between male circumcision and HIV status may be reflective of sociocultural factors that help protect men against HIV. For females, multiple sexual partnerships, time elapsed since sexual debut, place of residence, marital status, SES and regional prevalence of male circumcision were associated with HIV status. Moreover, there appear to be significant regional-level random effects for female adolescents. Efforts to stem the spread of HIV should be comprehensive, reflecting a reasonable balance between male circumcision, behaviour-change interventions and structural approaches. A human-rights approach is particularly indicated for female adolescents.
The author Stella Babalola (PhD) is a senior research advisor at the Johns Hopkins University Center for Communication Programs

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(JHU/CCP). She is also an associate professor and teaches health communication in the Department of Health, Behavior and Society at JHU. During the last five years, her research has been largely in the area of HIV-risk reduction, childhood immunisation, and adolescent reproductive health.

References
Abebe, Y., Schaap, A., Mamo, G., Negussie. A., Darimo, B., Wolday, D. & Sanders, E.J. (2003) HIV prevalence in 72 000 urban and rural male army recruits, Ethiopia. AIDS 17(12), pp. 18351840. Adimora, A.A. & Auerbach, J. (2010) Structural interventions for HIV prevention in the United States. Journal of Acquired Immune Deficiency Syndromes 55(supplement 2), pp. S132S135. Ahuja, A., Wendell, B. & Werker, E. (2006) Male Circumcision and AIDS: The Macroeconomic Impact of a Health Crisis. Boston, Massachusetts, Harvard Business School Working Paper 07-025. Auerbach, J.D., Parkhurst, J.O., Cceres, C.F. & Keller, K.E. (2009) Addressing Social Drivers of HIV/AIDS: Some Conceptual, Methodological, and Evidentiary Considerations . aids2013 Working Paper No. 24. New York, aids2031 Social Drivers Working Group. Brnighausen, T., Hosegood, V., Timaeus, I.M. & Newell, M.-L. (2007) The socioeconomic determinants of HIV incidence: evidence from a longitudinal, population-based study in rural South Africa. AIDS 21(supplement 7), pp. S29S38. Beegle, K. & De Walque, D. (2009) Demographic and Socioeconomic Patterns of HIV/AIDS Prevalence in Africa. October 2009, Policy Research Working Paper 5076. Washington, D.C., The World Bank Development Research Group Poverty and Inequality Team, and Human Development and Public Services Team. Boerma, J.T. & Weir, S.S. (2005) Integrating demographic and epidemiological approaches to research on HIV/AIDS: the proximate-determinants framework. The Journal of Infectious Diseases 191(supplement 1), pp. S61S67. Bongaarts, J. (1978) A framework for analyzing the proximate determinants of fertility. Population and Development Review 4(1), pp. 105132. Clark, S. (2004) Early marriage and HIV risks in southern Africa. Studies in Family Planning 35(3), pp. 149160. Clark, S., Bruce, J. & Dude, A. (2006) Protecting girls from HIV/ AIDS: the case against child and adolescent marriages. International Family Planning Perspectives 32(2), pp. 7988. Corno, L. & De Walque, D. (2007) The determinants of HIV infection and related sexual behaviors: evidence from Lesotho. World Bank Policy Research Working Paper Series 4421. Washington, D.C., The World Bank. Davis, K. & Blake, J. (1956) Social structure and fertility: an analytical framework. Economic Development and Cultural Change 4(3), pp. 211235. De Walque, D. (2009) Does education affect HIV status? Evidence from five African countries. World Bank Economic Review 23(2), pp. 209233. Dunkle, K.L., Stephenson, R., Karita, E., Chomba, E., Kayitenkore, K., Vwalika, C., Greenberg, L. & Allen, S. (2008) New heterosexually transmitted HIV infections in married or cohabiting couples in urban Zambia and Rwanda: an analysis of survey and clinical data. The Lancet 371(9631), pp. 21832191. Fortson, J.G. (2008) The gradient in sub-Saharan Africa: socioeconomic status and HIV/AIDS. Demography 45(2), pp. 303322. Fox, A.M. (2010) The social determinants of HIV serostatus in sub-Saharan Africa: an inverse relationship between poverty and

HIV? Public Health Reports 125(supplement 4), pp. S16S24. Gay, J., Hardee, K., Croce-Galis, M., Kowalski, S., with Gutari, C., Wingfield, C., Rovin, K. & Berzin, K. (2010) What Works for Women and Girls: Evidence for HIV/AIDS Interventions. June 2010. New York, Open Society Institute. Gillespie, S., Kadiyala, S. & Greener, R. (2007) Is poverty or wealth driving HIV transmission? AIDS 21(supplement 7), pp. S5S16. Glynn, J.R., Caral, M., Buv, A., Anagonou, S., Zekeng, L., Kahindo, M. & Musonda, R. (2004) Does increased general schooling protect against HIV infection? A study in four African cities. Tropical Medicine and International Health 9(1), pp. 414. Glynn, J.R., Sonnenberg, P., Nelson, G., Bester, A., Shearer, S. & Murray, J. (2007) Survival from HIV-1 seroconversion in southern Africa: a retrospective cohort study in nearly 2 000 gold-miners over 10 years of follow-up. AIDS 21(5), pp. 625632. Gouws, E., Staneckib, K.A., Lyerlaa, R. & Ghys, P.D. (2008) The epidemiology of HIV infection among young people aged 1524 years in southern Africa. AIDS 22(supplement 4), pp. S5S16. Guo, G. & Zhao, H. (2000) Multilevel modeling for binary data. Annual Review of Sociology 26, pp. 441462. Halperin, D. & Epstein, H. (2007) Why is HIV prevalence so severe in southern Africa? The role of multiple concurrent partnerships and lack of male circumcision: implications for AIDS prevention. Southern African Journal of HIV Medicine 8(1), pp. 1925. Jukes, M., Simmons, S. & Bundy, D. (2008) Education and vulnerability: the role of schools in protecting young women and girls from HIV in southern Africa. AIDS 22(supplement 4), pp. S41S56. Kayirangwa, E., Hanson, J., Munyakazi, L. & Kabeja, A. (2006) Current trends in Rwandas HIV/AIDS epidemic. Sexually Transmitted Infections 82(supplement 1), pp. i27i31. Kirunga, C.T. & Ntozi, J.P. (1997) Socio-economic determinants of HIV serostatus: a study in Rakai district, Uganda. Health Transition Review 7(supplement), pp. S175S188. Krishnan, S., Dunbar, M.S., Minnis, A.M., Medlin, C.A., Gerdts, C.E. & Padian, N.S. (2008) Poverty, gender inequities, and womens risk of human immunodeficiency virus/AIDS. Annals of the New York Academy of Sciences 1136(1), pp. 101110. Lachaud, J.P. (2007) HIV prevalence and poverty in Africa: microand macro-econometric evidences applied to Burkina Faso. Journal of Health Economics 26(3), pp. 483504. Lewis, J.J., Donnelly, C.A., Mare, P., Mupambireyi, Z., Garnett, G.P. & Gregson, S. (2007) Evaluating the proximate determinants framework for HIV infection in rural Zimbabwe. Sexually Transmitted Infections 83(supplement 1), pp. i61i69. Mishra, V., Barrere, B., Hong, R. & Kahn, S. (2008) Evaluation of bias in HIV seroprevalence estimates from national household surveys. Sexually Transmitted Infections 84(supplement 1), pp. i63i70. Mishra, V. & Bignami-Van Assche, S. (2009) Concurrent Sexual Partnerships and HIV Infection: Evidence from National Population-Based Surveys. DHS Working Paper No. 62. Calverton, Maryland, Macro International Inc. Mishra, V., Medley, A., Hong, R., Gu, Y. & Robey, B. (2009) Levels and Spread of HIV Seroprevalence and Associated Factors: Evidence from National Household Surveys. DHS Comparative Reports No. 22. Calverton, Maryland, Macro International Inc. Moses, S., Bradley, J.E., Nagelkerke, N.J.D., Ronald, A.R., NdinyaAchola, J.O. & Plummer, F.A. (1990) Geographical patterns of male circumcision practices in Africa: association with HIV seroprevalence. International Journal of Epidemiology 19(3), pp. 693697. Mosley, W.H. & Chen, L.C. (1984) An analytic framework for the study of child survival in developing countries. Population and Development Review 10(supplement), pp. 2545.

Downloaded by [210.57.215.150] at 19:55 06 March 2014

414

Babalola

Downloaded by [210.57.215.150] at 19:55 06 March 2014

Muula, A.S. (2006) On evidence in support of male circumcision in HIV prevention: What next? PLoS Medicine 3(1); doi: 10.1371/ journal.pmed.0030066. Pettifor, A., Rees, H., Kleinschmidt, I., Steffenson, A., MacPhail, C., Hlongwa-Madikizela, L., Vermaak, K. & Padian, N. (2005) Young peoples sexual health in South Africa: HIV prevalence and sexual behaviours from a nationally representative household survey. AIDS 19(14), pp. 15251534. Quinn, T.C. (2007) Circumcision and HIV transmission (Review). Current Opinion in Infectious Diseases 20(1), pp. 3338. Rabe-Hesketh, S. & Skrondal, A. (2008) Multilevel and Longitudinal Modeling Using Stata (2nd edition). College Station, Texas, Stata Press. Rabe-Hesketh, S., Skrondal, A. & Pickles, A. (2004) GLLAMM Manual (2nd edition). Berkeley, California, U.C. Berkeley Division of Biostatistics Working Paper Series, Paper No. 160. Shafii, T., Stovel, K., Davis, R. & Holmes, K. (2004) Is condom use habit forming? Condom use at sexual debut and subsequent condom use. Sexually Transmitted Diseases 31(6), pp. 366372. Shisana, O., Zungu-Dirwayi, N., Toefy, Y., Simbayi, L.C., Malik, S. & Zuma, K. (2004) Marital status and risk of HIV infection in South Africa. South African Medical Journal 94(7), pp. 537543. Smith, D.K., Taylor, A., Kilmarx, P.H., Sullivan, P., Warner, L., Kamb, L., Bock, N., Kohmescher, B. & Mastro, T.D. (2010) Male circumcision in the United States for the prevention of HIV infection and other adverse health outcomes: report from a CDC consultation. Public Health Reports 125(supplement 1), pp. 7282. Todd, J., Glynn, J.R., Marston, M., Lutalo, T., Biraro, S., Mwita, W., Suriyanon, V., Rangsin, R., Nelson, K.E., Sonnenberg, P., Fitzgerald, D., Karita, E. & Zaba, B. (2007) Time from HIV seroconversion to death: a collaborative analysis of eight studies in six low- and middle-income countries before highly active antiretroviral therapy. AIDS 21(supplement 6), pp. S55S63.

UNAIDS (2010) UNAIDS Report on the Global AIDS Epidemic 2010. Geneva, UNAIDS. Van Griensven, F., Varangrat, A., Wimonsate, W., Tanpradech, S., Kladsawad, K., Chemnasiri, T., Suksripanich, O., Phanuphak, P., Mock, P., Kanggarnrua, K., McNicholl, J. & Plipat, T. (2010) Trends in HIV prevalence, estimated HIV incidence, and risk behavior among men who have sex with men in Bangkok, Thailand, 20032007. Journal of Acquired Immune Deficiency Syndromes 53(2), pp. 234239. Weller, S.C. & Davis-Beaty, K. (2002) Condom effectiveness in reducing heterosexual HIV transmission. Cochrane Database of Systematic Reviews, Issue 1, Art. No.: CD003255; doi: 10.1002/14651858.CD003255. Wilson, C., Wright, P., Safrit, J. & Rudy, B. (2010) Epidemiology of HIV infection and risk in adolescents and youth. Journal of Acquired Immune Deficiency Syndromes 54(supplement 1), pp. S5S6. Wojcicki, J.M. (2005) Socioeconomic status as a risk factor for HIV infection in women in East, Central and Southern Africa: a systematic review. Journal of Biosocial Science 37(1), pp. 136. Yotebieng, M., Halperin, C.T., Mitchell, E.M. & Adimora, A.A. (2009) Correlates of condom use among sexually experienced secondary-school male students in Nairobi, Kenya. Journal of Social Aspects of HIV/AIDS 6(1), pp. 916. Zaba, B., Boerma, T. & White, R. (2000) Monitoring the AIDS epidemic using HIV prevalence data among young women attending antenatal clinics: prospects and problems. AIDS 14(11), pp. 16331645.